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First published online August 9, 2007
Journal of Experimental Biology 210, 2912-2922 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006874

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Sensory-induced modification of two motor patterns in the crab, Cancer pagurus

Carmen R. Smarandache and Wolfgang Stein^*

Institute of Neurobiology, Ulm University, D-89069 Ulm, Germany

View larger version (57K): [in this window] [in a new window]   Fig. 1. Morphological and electrophysiological identification of the AGR. (A) Schematic drawing of isolated STNS with gastric muscles gm1 and gm4a,b. The bipolar cell body of the sensory neuron AGR is located immediately posterior to the cell bodies of the motor neurons in the STG and projects one axon via the dgn and agn to the gm1 muscles and one axon via the stn and sons to the CoGs. (B) Lucifer Yellow fill of AGR showing the location of the AGR soma in the STG. AGR possessed no arborization in the STG neuropil. (C) Two spike initiation zones contributed to AGR spontaneous spike activity. Top: multisweep recordings (n=56 sweeps) of agn, stn and son, triggered on the AGR action potential on agn. The AGR spike could be seen on all recordings. Bottom: 149 sweeps of agn, stn and son, triggered on the AGR action potential on stn. CoG, commissural ganglion; OG, oesophageal ganglion; STG, stomatogastric ganglion; AGR, anterior gastric receptor; agn, anterior gastric receptor nerve; aln, anterior lateral nerve; dgn, dorsal gastric nerve; dvn, dorsal ventricular nerve; ion, inferior oesophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mvn, median ventricular nerve; son, superior oesophageal nerve; stn, stomatogastric nerve.

View larger version (14K): [in this window] [in a new window]   Fig. 2. AGR responds to tension increase in gm1 muscles. (A) Extracellular recording of AGR on dgn during passive stretch of a gm1 muscle. Stretch was applied by moving the ossicle between the gm1 and gm4 muscles in the posterior direction. AGR firing frequency increased during the stretch (top trace). (B) Extracellular recording of AGR on agn during isometric contraction of a gm1 muscle. Anterior and posterior muscle attachment sites were fixed to the Sylgard® such that the muscle attained its resting length (measured beforehand in the intact animal). During spontaneous gastric mill rhythms, activity of the GM motor neurons (bottom trace) activated AGR. Before GM activity, the AGR spike initiation zone in the stn was active. During GM activity, the spike initiation zone close to the muscle became active (*). The top trace shows AGR firing frequency in this condition. See text for definition of abbreviations.

View larger version (25K): [in this window] [in a new window]   Fig. 3. The anterior gastric receptor (AGR) shows spike frequency adaptation and sag potential. (A) Intracellular recording of AGR. AGR was depolarized with current injections. Bottom, +1 nA; middle, +3 nA; top trace, adaptation of AGR firing frequency during current injections. After an initial peak, firing frequencies dropped to constant value. (B) Current injections were used to hyperpolarize AGR to different membrane potentials. After an early hyperpolarized peak, the membrane potential decayed to a constant value (sag). After the end of the hyperpolarization, the membrane potential transiently overshot the resting potential and AGR firing frequencies increased (top trace).

View larger version (41K): [in this window] [in a new window]   Fig. 4. AGR affects the pyloric rhythm. (A) Intracellular recordings of AGR and LG and extracellular recordings of three pyloric nerves. AGR was depolarized with current injection. While the spike activities of IC and VD were diminished during the depolarization, LG was activated by the stimulus. (B) Mean number of spikes per burst of the pyloric neurons PD, LP, VD and IC, and pyloric cycle period before (open boxes) and during AGR stimulation (filled boxes) when LG was active. **P<0.01. (C) Same experiment as in A. Current injection was used to prevent spike activity in LG. (D) On average, IC and VD activity was diminished during AGR activity, even when LG was not active. In addition, the pyloric period increased. *P<0.05. See text for definition of abbreviations.

View larger version (23K): [in this window] [in a new window]   Fig. 5. Influence of AGR on gastric mill motor neurons. (A) Intracellular recordings of the gastric mill neurons GM, LG and DG. Superposition of five sweeps during AGR stimulation, triggered at the beginning of the AGR stimulus. LG and GM were excited during the AGR stimulation, DG received hyperpolarization. (B) In low-Ca2+-saline, LG received at least two different types of electrical PSPs. Before and after AGR activity, large PSPs were present (i). During AGR activity, these large PSPs disappeared and small PSPs showed up (ii). During the course of the stimulation, the large PSPs reappeared and elicited action potentials (arrow). Horizontal scale bars in i and ii, 0.2 s; vertical, 1 mV). See text for definition of abbreviations.

View larger version (26K): [in this window] [in a new window]   Fig. 6. LG shows no inactivation during strong AGR firing. (A) Response of LG to AGR depolarization with different currents (bottom, +5 nA; middle, +1 nA; top, +0.5 nA). AGR activity is shown as instantaneous firing frequency. (B) Plot of LG intraburst firing frequency over AGR firing frequency. (C) In preparations without spontaneous gastric mill rhythms, rhythmic AGR stimulation elicited a gastric mill rhythm which included activity of pro- (LG, GM) and retractor motor neurons (DG). See text for definition of abbreviations.

View larger version (41K): [in this window] [in a new window]   Fig. 7. Influence of AGR on spontaneous gastric mill rhythms. (A) Entrainment of a gastric mill rhythm with rhythmic activation of AGR. Original recordings of lgn and intracellular recording of AGR. Top: control, AGR was not stimulated. Middle: AGR was stimulated with a period of 5 s. The gastric mill rhythm was entrained to the stimulus. Bottom: stimulation of AGR with a period longer than control (8 s). The period of the rhythm corresponded to that of the stimulation. (B) Entrainment of the gastric mill rhythm. Mean of N=11 animals. The period of the rhythm is plotted over stimulation period. Both parameters are normalized to the period of the spontaneous rhythm (control). Linear regression between 0.4 and 1.6 stimulation period, R2=0.99. GMR, gastric mill rhythm. (C) Response of LG to a single burst of AGR during a spontaneous gastric mill rhythm. The AGR burst shortened the expected cycle period (phase advance). (D) Mean phase response curve of LG. AGR stimulation was capable of resetting the rhythm at any phase of the cycle. Linear regression, R2=0.95. See text for definition of abbreviations